Rajidae

Gérard, Claudia, Trochard, Caroline, Hervé, Maxime R., Hamel, Héloïse, Gay, Mélanie, Barbier, Michel, Trancart, Thomas & Barreau, Thomas, 2024, Communities of metazoan parasites in seven sympatric skate species (Elasmobranchii, Rajidae) from the English Channel and Celtic Sea differing in conservation status, Journal of Fish Biology 105 (3), pp. 975-987 : 983-984

4.1 | Parasite component communities of Rajidae and comparison with previous studies

Comparison with previous parasitological surveys (e.g., Alvarez ´ et al., 2006; McVicar, 1977; Sanmartín et al., 2000) is difficult because of differences in methods (fish previously frozen before parasitological examination in our study vs. freshly euthanized), but also in sampling effort, areas, and timing that can at least partially account for some differences between the component communities of metazoan parasites. In particular, the freezing of skates before parasite research can partly explain why we found far fewer platyhelminths such as cestodes and monogeneans than in previous surveys. Indeed, these soft-bodied helminths can be damaged or even destroyed by the ice crystals formed during freezing, in contrast to nematodes that are highly resistant to freezing due to their protective outer cuticle and were dominant in our study. However, despite research on defrosted skates and relatively low sampling size, our exploratory study revealed 16 new host–parasite associations in Rajidae from the English Channel and Celtic Sea, among them 10 involving nematodes (Table 2).

In the case of L. fullonica , despite the lack of a specific parasitological study and other data on prevalences, at least 11 species among them eight platyhelminths were registered according to the online bibliographical database of Pollerspöck and Straube (2023) and Williams (1964), versus five in our study, among them four new records, i.e., the three nematode taxa ( A. simplex , Phocanema spp. , and Proleptus sp. ) and an unidentified gill myxosporean. Concerning L. naevus , 19 species of metazoan parasites were listed by Pollerspöck and Straube (2023), and 14 parasite taxa of which eight platyhelminths occurred with a prevalence of 100% in the 263 L. naevus studied by McVicar (1977) in British waters including the English Channel, whereas 47% of our 14 specimens were infected by six taxa. Among them, only two cestodes, Echeneibothrium spp. and Grillotia erinaceus , were in common; A. simplex , previously considered accidental, was the most prevalent species in our study, and we recorded Phocanema spp. for the first time in L. naevus . Note that recent taxonomical studies by Bao et al. (2023) have resulted in the resurrection of the genus Phocanema , previously included in the genus Pseudoterranova . On the northwest coast of Spain, both Raja brachyura (60 individuals) and Raja microocellata (52) harbored 18 parasite taxa with prevalences up to 92% and 96%, respectively (Alvarez ´et al., 2006), versus respectively three and seven taxa in R. brachyura (21 individuals) and R. microocellata (14) in our study in the northeast Atlantic with overall prevalences of 29% and 93%. Phocanema azarasi , Phocanema krabbei and an unidentified gill myxosporean were registered for the first time in R. microocellata ; no new records occurred for R. brachyura . Note that 28 and 24 species of metazoan parasites, respectively, were listed in R. brachyura and R. microocellata by Pollerspöck and Straube (2023). Concerning Raja undulata , among the 17 parasite species enumerated by Pollerspöck and Straube (2023), 16 were recorded with a total prevalence of 99% in 78 individuals from the northwest coast of Spain (Alvarez ´et al., 2006; Sanmartín et al., 2000). Among them, only the cestode Onchobothrium spp. was found in our 14 R. undulata studied, of which 79% were parasitized. In total, we detected six parasite taxa in R. undulata , including five new records, i.e., P. azarasi and P. krabbei , the cestodes Rockacestus sp. and Nybelinia spp. , and an unidentified gill myxosporean. Parasite diversity was also higher in the six Spanish R. montagui studied by Alvarez ´et al. (2006) harboring seven parasite taxa (prevalence not available), compared to our 21 specimens from the northeast Atlantic parasitized with a total prevalence of 19% by three taxa, including the new record of Phocanema spp. According to Pollerspöck and Straube (2023), 22 species of metazoan parasites have been registered in R. montagui . For R. clavata , despite 71 parasite species listed by Pollerspöck and Straube (2023) (even if all of these are probably not valid), only four taxa were recorded in the 28 skates from the west coast of Ireland studied by Henderson and Dunne (1999) as in our 20 individuals. Proleptus sp. was the single parasite taxon recorded in both studies with respective prevalences of 21% and 30%. Interestingly, no cestodes occurred in Irish R. clavata ( Henderson & Dunne, 1999) , despite at least 27 species mentioned in the database of Pollerspöck and Straube (2023). In addition to Proleptus sp. , we found two cestode species, Echeneibothrium spp. and Tritaphros retzii , in R. clavata , and A. simplex recorded for the first time.

Notwithstanding the fact that we recorded 16 new host–parasite associations, the parasite communities we described in skates from the English Channel and Celtic Sea appeared depauperate. As previously evoked, this could be partially explained by the possible loss of soft-bodied helminths due to freezing and our lower sampling effort, but it could also reflect environmental changes over time, encompassing a potential decrease of free-living biodiversity affecting heteroxenous parasites such as trophically transmitted helminths (e.g., Hatcher et al., 2012; Hudson et al., 2006; Marcogliese, 2005; Timi & Poulin, 2020 for reviews). Intensive fishing can drive declines in fish parasite diversity, especially trophically transmitted parasites that require multiple host species, some of which are the top predators most sensitive to fishing impacts ( Wood et al., 2014). In this way, MacKenzie & Pert (2018) showed evidence for the decline and possible extinction of a digenean parasite species caused by intensive fishing of the near-threatened Raja clavata , suggesting that the population size of the final host was below the threshold required for successful transmission of the parasite. Differences between parasite component communities can also originate from differences in sampling areas potentially inhabited by different intermediate, paratenic, and/or definitive host species, as observed for R. undulata between the continental shelf and the estuary of Muros–Noia in northwest Spain (Alvarez ´et al., 2006; Sanmartín et al., 2000). Our record of 16 new host–parasite associations involving Rajidae may also result from modifications of both abiotic conditions and biocenoses in the context of global change. Indeed, water temperatures in the English Channel and Celtic Sea have increased 0.17–0.45 C per decade between 1985 and 2014, with consequences on free-living species from plankton to seabirds ( Hughes et al., 2017; Lauria et al., 2013). Moreover, the occurrence of both Phocanema spp. , the dominant parasite taxon of our study and firstly recorded in Rajidae (i.e., L. fullonica , L. naevus , R. microocellata , R. montagui , and R. undulata ), and

Rajidae Fish Decapods Other crustaceans Cephalopods Other mollusks Polychetes

Leucoraja fullonica 65.46 22.15 6.82

Leucoraja naevus 45.57 20.31 19.17

Raja brachyura 34.32 25.58 35.13

Raja clavata 21.03 55.37 14.02

Raja microocellata 49.21 46.39 1.69

Raja montagui 6.17 65.11 17.83

Raja undulata 7.90 91.64 0

A. simplex , newly recorded in L. fullonica and R. clavata , may confirm the increase of anisakiasis observed worldwide ( Fiorenza et al., 2020; Mattiucci et al., 2017). It raises the question of anisakiasis risk for human consumption, as the genera most often associated with anisakiasis are Anisakis and Pseudoterranova ( Chai et al., 2005 for review), the latter now divided in two distinct genera, Pseudoterranova and Phocanema ( Bao et al., 2023) .